Characterization of axon guidance cue sensitivity of human embryonic stem cell-derived dopaminergic neurons

Molecular and Cellular Neuroscience

Volumn 45, Issue 4, 2010, Pages 324-334

  Cord, Branden J ^a   Li, Jie ^a   Works, Melissa ^a   McConnell, Susan K ^a   Palmer, Theo ^a   Hynes, Mary A ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Axon guidance; Cytokine; Dopaminergic neuron; Netrin; Parkinson's disease; Slit; Substantia nigra

Indexed keywords

CELL PROTEIN; HEPATOCYTE NUCLEAR FACTOR 3BETA; NETRIN 1; PROTEIN EN 1; PROTEIN NURR 1; SLIT2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN DISEASE; CELL MATURATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SUBSTANTIA NIGRA;

AXONS; CELL DIFFERENTIATION; CELL LINE; CUES; DOPAMINE; EMBRYONIC STEM CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; NEUROGENESIS; NEURONS;

RODENTIA;

EID: 77957941338     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.07.004     Document Type: Article

References (48)

1. Andrews W., Liapi A., Plachez C., Camurri L., Zhang J., Mori S., Murakami F., Parnavelas J.G., Sundaresan V., Richards L.J. Robo1 regulates the development of major axon tracts and interneuron migration in the forebrain. Development (Cambridge, England) 2006, 133:2243-2252.
2. Bagri A., Marin O., Plump A.S., Mak J., Pleasure S.J., Rubenstein J.L., Tessier-Lavigne M. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 2002, 33:233-248.
3. Barker R.A., Fricker R.A., Abrous D.N., Fawcett J., Dunnett S.B. A comparative study of preparation techniques for improving the viability of nigral grafts using vital stains, in vitro cultures, and in vivo grafts. Cell Transplant. 1995, 4:173-200.
4. Bonilla S., Hall A.C., Pinto L., Attardo A., Gotz M., Huttner W.B., Arenas E. Identification of midbrain floor plate radial glia-like cells as dopaminergic progenitors. Glia 2008, 56:809-820.
5. Braisted J.E., Catalano S.M., Stimac R., Kennedy T.E., Tessier-Lavigne M., Shatz C.J., O'Leary D.D. Netrin-1 promotes thalamic axon growth and is required for proper development of the thalamocortical projection. J. Neurosci. 2000, 20:5792-5801.
6. Chen Z., Palmer T.D. Cellular repair of CNS disorders: an immunological perspective. Hum. Mol. Genet. 2008, 17:R84-R92.
7. Crossley P.H., Martinez S., Martin G.R. Midbrain development induced by FGF8 in the chick embryo. Nature 1996, 380:66-68.
8. Davis C.A., Joyner A.L. Expression patterns of the homeo box-containing genes En-1 and En-2 and the proto-oncogene int-1 diverge during mouse development. Genes Dev. 1988, 2:1736-1744.
9. Dunnett S.B. Towards a neural transplantation therapy for Parkinson's disease: experimental principles from animal studies. Acta Neurochir. Suppl. (Wien) 1991, 52:35-38.
10. Elkabetz Y., Panagiotakos G., Al Shamy G., Socci N.D., Tabar V., Studer L. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev. 2008, 22:152-165.
11. Furne C., Rama N., Corset V., Chedotal A., Mehlen P. Netrin-1 is a survival factor during commissural neuron navigation. Proc. Natl. Acad. Sci. USA 2008, 105:14465-14470.
12. Gadient R.A., Lachmund A., Unsicker K., Otten U. Expression of interleukin-6 (IL-6) and IL-6 receptor mRNAs in rat adrenal medulla. Neurosci. Lett. 1995, 194:17-20.
13. Guan K., Chang H., Rolletschek A., Wobus A.M. Embryonic stem cell-derived neurogenesis. Retinoic acid induction and lineage selection of neuronal cells. Cell Tissue Res. 2001, 305:171-176.
14. Hamasaki T., Goto S., Nishikawa S., Ushio Y. A role of netrin-1 in the formation of the subcortical structure striatum: repulsive action on the migration of late-born striatal neurons. J. Neurosci. 2001, 21:4272-4280.
15. Hammond R., Blaess S., Abeliovich A. Sonic hedgehog is a chemoattractant for midbrain dopaminergic axons. PLoS ONE 2009, 4:e7007.
16. Hansson S.R., Hoffman B.J., Mezey E. Ontogeny of vesicular monoamine transporter mRNAs VMAT1 and VMAT2. I. The developing rat central nervous system. Brain Res. Dev. Brain Res. 1998, 110:135-158.
17. Hernandez-Montiel H.L., Tamariz E., Sandoval-Minero M.T., Varela-Echavarria A. Semaphorins 3A, 3C, and 3F in mesencephalic dopaminergic axon pathfinding. J. Comp. Neurol. 2008, 506:387-397.
18. Hynes M., Porter J.A., Chiang C., Chang D., Tessier-Lavigne M., Beachy P.A., Rosenthal A. Induction of midbrain dopaminergic neurons by Sonic hedgehog. Neuron 1995, 15:35-44.
19. Ihara S., Iwamatsu A., Fujiyoshi T., Komi A., Yamori T., Fukui Y. Identification of interleukin-6 as a factor that induces neurite outgrowth by PC12 cells primed with NGF. J. Biochem. 1996, 120:865-868.
20. Jankovic J. An update on the treatment of Parkinson's disease. Mt. Sinai J. Med. 2006, 73:682-689.
21. Kittappa R., Chang W.W., Awatramani R.B., McKay R.D. The foxa2 gene controls the birth and spontaneous degeneration of dopamine neurons in old age. PLoS Biol. 2007, 5:e325.
22. Klar A., Baldassare M., Jessell T.M. F-spondin: a gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell 1992, 69:95-110.
23. Kolk S.M., Gunput R.A., Tran T.S., van den Heuvel D.M., Prasad A.A., Hellemons A.J., Adolfs Y., Ginty D.D., Kolodkin A.L., Burbach J.P., Smidt M.P., Pasterkamp R.J. Semaphorin 3F is a bifunctional guidance cue for dopaminergic axons and controls their fasciculation, channeling, rostral growth, and intracortical targeting. J. Neurosci. 2009, 29:12542-12557.
24. Lee, H.S., Bae, E.J., Yi, S.H., Shim, J.W., Jo, A.Y., Kang, J.S., Yoon, E.H., Rhee, Y.H., Park, C.H., Koh, H.C., Kim, H.J., Choi, H.S., Han, J.W., Lee, Y.S., Kim, J., Li, J.Y., Brundin, P., Lee, S.H., Foxa2 and Nurr1 synergistically yield A9 nigral dopamine neurons exhibiting improved differentiation, function, and cell survival. Stem Cells (Dayton, Ohio) 28, 501-512.
25. Lin L., Isacson O. Axonal growth regulation of fetal and embryonic stem cell-derived dopaminergic neurons by Netrin-1 and Slits. Stem Cells (Dayton, Ohio) 2006, 24:2504-2513.
26. Lin L., Rao Y., Isacson O. Netrin-1 and slit-2 regulate and direct neurite growth of ventral midbrain dopaminergic neurons. Mol. Cell. Neurosci. 2005, 28:547-555.
27. Ling Z.D., Potter E.D., Lipton J.W., Carvey P.M. Differentiation of mesencephalic progenitor cells into dopaminergic neurons by cytokines. Exp. Neurol. 1998, 149:411-423.
28. Marillat V., Cases O., Nguyen-Ba-Charvet K.T., Tessier-Lavigne M., Sotelo C., Chedotal A. Spatiotemporal expression patterns of slit and robo genes in the rat brain. J. Comp. Neurol. 2002, 442:130-155.
29. McCaffery P., Drager U.C. High levels of a retinoic acid-generating dehydrogenase in the meso-telencephalic dopamine system. Proc. Natl. Acad. Sci. USA 1994, 91:7772-7776.
30. Muller F., O'Rahilly R. The development of the human brain, the closure of the caudal neuropore, and the beginning of secondary neurulation at stage 12. Anat. Embryol. (Berl.) 1987, 176:413-430.
31. Nakamura M., Houghtling R.A., MacArthur L., Bayer B.M., Bregman B.S. Differences in cytokine gene expression profile between acute and secondary injury in adult rat spinal cord. Exp. Neurol. 2003, 184:313-325.
32. Okada A., Charron F., Morin S., Shin D.S., Wong K., Fabre P.J., Tessier-Lavigne M., McConnell S.K. Boc is a receptor for sonic hedgehog in the guidance of commissural axons. Nature 2006, 444:369-373.
33. Parish C.L., Finkelstein D.I., Tripanichkul W., Satoskar A.R., Drago J., Horne M.K. The role of interleukin-1, interleukin-6, and glia in inducing growth of neuronal terminal arbors in mice. J. Neurosci. 2002, 22:8034-8041.
34. Perrier A.L., Tabar V., Barberi T., Rubio M.E., Bruses J., Topf N., Harrison N.L., Studer L. Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 2004, 101:12543-12548.
35. Sasai Y. Directed differentiation of neural and sensory tissues from embryonic stem cells in vitro. Ernst Schering Res. Found. Workshop 2005, 101-109.
36. Savitt J.M., Dawson V.L., Dawson T.M. Diagnosis and treatment of Parkinson disease: molecules to medicine. J. Clin. Investig. 2006, 116:1744-1754.
37. Schulz T.C., Noggle S.A., Palmarini G.M., Weiler D.A., Lyons I.G., Pensa K.A., Meedeniya A.C., Davidson B.P., Lambert N.A., Condie B.G. Differentiation of human embryonic stem cells to dopaminergic neurons in serum-free suspension culture. Stem Cells (Dayton, Ohio) 2004, 22:1218-1238.
38. Simon H.H., Thuret S., Alberi L. Midbrain dopaminergic neurons: control of their cell fate by the engrailed transcription factors. Cell Tissue Res. 2004, 318:53-61.
39. Sriram K., Matheson J.M., Benkovic S.A., Miller D.B., Luster M.I., O'Callaghan J.P. Mice deficient in TNF receptors are protected against dopaminergic neurotoxicity: implications for Parkinson's disease. FASEB J. 2002, 16:1474-1476.
40. Suli A., Mortimer N., Shepherd I., Chien C.B. Netrin/DCC signaling controls contralateral dendrites of octavolateralis efferent neurons. J. Neurosci. 2006, 26:13328-13337.
41. Tanaka D.H., Yamauchi K., Murakami F. Guidance mechanisms in neuronal and axonal migration. Brain Nerve 2008, 60:405-413.
42. Temporin K., Tanaka H., Kuroda Y., Okada K., Yachi K., Moritomo H., Murase T., Yoshikawa H. Interleukin-1 beta promotes sensory nerve regeneration after sciatic nerve injury. Neurosci. Lett. 2008, 440:130-133.
43. Torre, E.R., Gutekunst, C.A., Gross, R.E., Expression by midbrain dopamine neurons of Sema3A and 3F receptors is associated with chemorepulsion in vitro but a mild in vivo phenotype. Mol. Cell. Neurosci. 44, 135-153.
44. Torres E.M., Dowd E., Dunnett S.B. Recovery of functional deficits following early donor age ventral mesencephalic grafts in a rat model of Parkinson's disease. Neuroscience 2008, 154:631-640.
45. Wallen A., Zetterstrom R.H., Solomin L., Arvidsson M., Olson L., Perlmann T. Fate of mesencephalic AHD2-expressing dopamine progenitor cells in NURR1 mutant mice. Exp. Cell Res. 1999, 253:737-746.
46. Yan Y., Yang D., Zarnowska E.D., Du Z., Werbel B., Valliere C., Pearce R.A., Thomson J.A., Zhang S.C. Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells (Dayton, Ohio) 2005, 23:781-790.
47. Yang F., Wang J.C., Han J.L., Zhao G., Jiang W. Different effects of mild and severe seizures on hippocampal neurogenesis in adult rats. Hippocampus 2008, 18:460-468.
48. Yue Y., Widmer D.A., Halladay A.K., Cerretti D.P., Wagner G.C., Dreyer J.L., Zhou R. Specification of distinct dopaminergic neural pathways: roles of the Eph family receptor EphB1 and ligand ephrin-B2. J. Neurosci. 1999, 19:2090-2101.